journal article·2024-03Open access

Micrometer-scale structure in shark vertebral centra

S.R. Stock, U. Kierdorf, K.C. James, P.D. Shevchenko, L.J. Natanson, S. Gomez, H. Kierdorf

Acta Biomaterialia· Volume 177

Abstract

The vertebral centra of sharks consist of cartilage, and many species' centra contain a bioapatite related to that in bone. Centra microarchitectures at the 0.5-50 µm scale do not appear to have been described previously. This study examines centrum microarchitecture in lamniform and carcharhiniform sharks with synchrotron microComputed Tomography (microCT), scanning electron microscopy and spectroscopy and light microscopy. The analysis centers on the blue shark (carcharhiniform) and shortfin mako (lamniform), species studied with all three modalities. Synchrotron microCT results from seven other species complete the report. The main centrum structures, the corpus calcareum and intermedialia, consist of fine, closely-spaced, mineralized trabeculae whose mean thicknesses and spacings range from 4.5 to 11.2 µm and 4.5 to 15.6 µm, respectively. A significant (p = 0.00001) positive linear relationship between and exists for multiple positions within one mako centrum. Carcharhiniform species' and exhibit an inverse linear relationship (p = 0.005) while in lamniforms these variables tend toward a positive relationship which does not reach statistical significance (p = 0.099). In all species, the trabeculae form an uninterrupted, interconnected network, and the unmineralized volumes are similarly interconnected. Small differences in mineralization level are observed in trabeculae. Centrum growth band pairs are found to consist of locally higher /lower mineral volume fraction. Within the intermedialia, radial canals and radial microrods were characterized, and compacted trabeculae are prominent in the mako intermedialia. The centra's mineralized central zones were non-trabecular and are also described. STATEMENT OF SIGNIFICANCE: This study's novel result is the demonstration that the mineralized cartilage of sharks' vertebral bodies (centra) consists of a fine 3D array of interconnected plates (trabeculae) and an interpenetrating network of unmineralized tissue. This microstructure is radically different from that in tesserae or in teeth, the other main mineralized shark tissues. Using volumetric synchrotron microComputed Tomography, numerical values of mean trabecular thickness and spacing and their relationship were measured for nine species. Scanning electron microscopy added a higher resolution view of the microstructures, and histology provided complementary information on cartilage and cells. The present results suggest centra microstructure helps accommodate the very large in vivo strains and may prevent damage accumulation during millions of cycles of swimming-induced loading.
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Research context

OpenAlex topics: Ichthyology and Marine Biology · Paleontology and Evolutionary Biology · Shape Memory Alloy Transformations

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (36)

Show source-provided references
1. The slowest fish: swim speed and tail-beat frequency of Greenland sharks10.1016/j.jembe.2012.04.021 ↗
2. Bioapatite in shark centra studied by wide angle and by small angle x-ray scattering10.1098/rsif.2022.0373 ↗
3. Built for speed: strain in the cartilaginous vertebral columns of sharks10.1016/j.zool.2013.10.007 ↗
4. Martin · 1998
5. Ultrastructural, material and crystallographic description of endophytic masses–a possible damage response in shark and ray tessellated calcified cartilage10.1016/j.jsb.2017.03.004 ↗
6. The material bone: structure-mechanical function relations10.1146/annurev.matsci.28.1.271 ↗
7. On the calcification of the vertebral centra in sharks and rays10.1098/rstb.1921.0008 ↗
8. Wurmbach, H. 1932. Das wachstum des selachierwirbels und seiner gewebe. Zool Jb Abt Anat Ontog Tiere 55, 1-136, plates 1, 2.
9. Skeletogenesis in the swell shark Cephaloscyllium ventriosum10.1111/j.1469-7580.2007.00723.x ↗
10. Bone-like features in skate suggest a novel elasmobranch synapomorphy and deep homology of trabecular mineralization patterns10.1016/j.actbio.2018.11.047 ↗
11. Mineralized cartilage and bone-like tissues in chondrichthyans offer potential insights into the evolution and development of mineralized tissues in the vertebrate endoskeleton10.3389/fgene.2021.762042 ↗
12. Diversity and evolution of mineralized skeletal tissues in chondrichthyans10.3389/fevo.2021.660767 ↗
13. Micro-computed tomography: an alternative method for shark aging10.1111/j.1095-8649.2011.03188.x ↗
14. Age and growth of sharks: do vertebral band pairs record age?10.1071/MF17279 ↗
15. Shark vertebral microanatomy and mineral density variation studied with laboratory microComputed Tomography10.1016/j.jsb.2022.107831 ↗
16. Three-dimensional mapping of mineral in intact shark centra with energy dispersive x-ray diffraction10.1016/j.jmbbm.2022.105506 ↗
17. Microstructure and energy dispersive diffraction reconstruction of 3D patterns of crystallographic texture in a shark centrum10.1117/1.JMI.9.3.031504 ↗
18. The multiscale architecture of tessellated cartilage and its relation to function10.1111/jfb.14444 ↗
19. Applying methods of hard tissues preparation for wood anatomy: imaging polished samples embedded in polymethylmethacrylate10.1016/j.dendro.2018.08.005 ↗
20. Real-time streaming tomographic reconstruction with on-demand data capturing and 3D zooming to regions of interest10.1107/S1600577522003095 ↗
21. Stock · 2019
22. BoneJ: free and extensible bone image analysis in ImageJ10.1016/j.bone.2010.08.023 ↗
23. Rasband, W., contributors. 2022. ImageJ, version 1.53t, http://imagej.nih.gov/ij.
24. Preparation of calcified tissues for light microscopy
25. Imaging hard – inside the skeleton
26. Smith · 1980
27. Mineralized cartilage in the skeleton of chondrichthyan fishes10.1016/j.zool.2006.03.002 ↗
28. Gibson · 1999
29. Lawrence Livermore National Laboratory · 1991 · 100
30. A framework relating macroscopic measures and physical processes of crack closure of Al-Li alloy 2090
31. Mechanical behavior of shark vertebral centra at biologically relevant strains10.1242/jeb.188318 ↗
32. The occurrence of cartilage canals in shark vertebrae10.1139/z82-069 ↗
33. Collagen mineralization: aspects of the structural relationship between collagen and apatitic crystallites10.1007/978-1-4613-1487-5_3 ↗
34. Aspects of collagen mineralization in hard tissue formation10.1016/S0074-7696(04)42003-8 ↗
35. Mechanical properties of sand tiger shark (Carcharias taurus) vertebrae in relation to spinal deformity
36. Dryad Data Repository. 2023. https://datadryad.org/stash, accessed 07/10/2023.